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Structural And Functional Organization Of The Synapse pp 173–204Cite as

Adhesion Molecules at the Synapse

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Abstract

Communication between neurons is mediated mainly by chemical synapses, at which neurotransmitters are released by the presynaptic neuron, diffuse across the narrow cleft, and activate receptors located on postsynaptic neurons. Synapses provide the structural and functional basis for the formation and maintenance of the complex neural networks that exist in the brain. This process is governed by the number, type, and location of synapses control synapse maturation, specificity and function. Thus, disruption of the adhesive properties of these molecules not only compromises synaptic transmission, but also many aspects of brain function that control memory formation and behavior. Here, I will describe the various stages of synaptogenesis, with focus on adhesion molecules that regulate contact initiation, synapse maturation/stabilization or elimination, and synaptic plasticity. Emphasis will be on the potential mechanisms that regulate adhesion molecule recruitment and function at the synapse. I will also discuss how dysfunction in specific adhesive systems may contribute to synaptic imbalance and the development of brain disorders.

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References

  1. Ahmari SE, Buchanan J, and Smith SJ. Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3: 445–451: 2000.

    PubMed  CAS  Google Scholar 

  2. Anderson TR, Shah PA, and Benson DL. Maturation of glutamatergic and GABAergic synapse composition in hippocampal neurons.Neuropharmacology 47: 694–705: 2004.

    PubMed  CAS  Google Scholar 

  3. Ango F, di Cristo G, Higashiyama H, Bennett V, Wu P, and Huang ZJ. Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 119: 257–272: 2004.

    PubMed  CAS  Google Scholar 

  4. Arami S, Jucker M, Schachner M, and Welzl H. The effect of continuous intraventricular infusion of L1 and NCAM antibodies on spatial learning in rats. Behav Brain Res 81: 81–87: 1996.

    PubMed  CAS  Google Scholar 

  5. Atasoy D, Schoch S, Ho A, Nadasy KA, Liu X, Zhang W, Mukherjee K, Nosyreva ED, Fernandez-Chacon R, Missler M, Kavalali ET, and Sudhof TC. Deletion of CASK in mice is lethal and impairs synaptic function. Proc Natl Acad Sci U S A 104: 2525–2530, 2007.

    PubMed  CAS  Google Scholar 

  6. Auranen M, Vanhala R, Varilo T, Ayers K, Kempas E, Ylisaukko-Oja T, Sinsheimer JS, Peltonen L, and Jarvela I. A genomewide screen for autism-spectrum disorders: evidence for a major susceptibility locus on chromosome 3q25-27. Am J Hum Genet 71: 777–790, 2002.

    PubMed  Google Scholar 

  7. Bamji SX, Shimazu K, Kimes N, Huelsken J, Birchmeier W, Lu B, and Reichardt LF. Role of beta-catenin in synaptic vesicle localization and presynaptic assembly. Neuron 40: 719–731: 2003.

    PubMed  CAS  Google Scholar 

  8. Barnard EA, Skolnick P, Olsen RW, Mohler H, Sieghart W, Biggio G, Braestrup C, Bateson AN, and Langer SZ. International Union of Pharmacology. XV. Subtypes of gamma-aminobutyric acidA receptors: classification on the basis of subunit structure and receptor function. Pharmacol Rev 50: 291–313: 1998.

    PubMed  CAS  Google Scholar 

  9. Benson DL and Tanaka H. N-cadherin redistribution during synaptogenesis in hippocampal neurons. J Neurosci 18: 6892–6904: 1998.

    PubMed  CAS  Google Scholar 

  10. Biederer T, Sara Y, Mozhayeva M, Atasoy D, Liu X, Kavalali ET, and Sudhof TC. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297: 1525–1531: 2002.

    PubMed  CAS  Google Scholar 

  11. Bliss T, Errington M, Fransen E, Godfraind JM, Kauer JA, Kooy RF, Maness PF, and Furley AJ. Long-term potentiation in mice lacking the neural cell adhesion molecule L1. Curr Biol 10: 1607–1610: 2000.

    PubMed  CAS  Google Scholar 

  12. Bolliger MF, Frei K, Winterhalter KH, and Gloor SM. Identification of a novel neuroligin in humans which binds to PSD-95 and has a widespread expression. Biochem J 356: 581–588: 2001.

    PubMed  CAS  Google Scholar 

  13. Boucard AA, Chubykin AA, Comoletti D, Taylor P, and Sudhof TC. A Splice Code for trans-Synaptic Cell Adhesion Mediated by Binding of Neuroligin 1 to alpha- and beta- Neurexins. Neuron 48: 229–236: 2005.

    PubMed  CAS  Google Scholar 

  14. Bowery NG, Bettler B, Froestl W, Gallagher JP, Marshall F, Raiteri M, Bonner TI, and Enna SJ. International Union of Pharmacology. XXXIII. Mammalian gammaaminobutyric acid(B) receptors: structure and function. Pharmacol Rev 54: 247–264, 2002.

    PubMed  CAS  Google Scholar 

  15. Bozdagi O, Valcin M, Poskanzer K, Tanaka H, and Benson DL. Temporally distinct demands for classic cadherins in synapse formation and maturation. Mol Cell Neurosci 27: 509–521: 2004.

    PubMed  CAS  Google Scholar 

  16. Bredt DS and Nicoll RA. AMPA receptor trafficking at excitatory synapses. Neuron 40: 361–379: 2003.

    PubMed  CAS  Google Scholar 

  17. Bresler T, Shapira M, Boeckers T,Dresbach T, Futter M, Garner CC, Rosenblum K, Gundelfinger ED, and Ziv NE. Postsynaptic density assembly is fundamentally different from presynaptic active zone assembly. J Neurosci 24: 1507–1520: 2004.

    PubMed  CAS  Google Scholar 

  18. Brose N. Synaptic cell adhesion proteins and synaptogenesis in the mammalian central nervous system. Naturwissenschaften 86: 516–524: 1999.

    PubMed  CAS  Google Scholar 

  19. Brunig I, Suter A, Knuesel I, Luscher B, and Fritschy JM. GABAergic terminals are required for postsynaptic clustering of dystrophin but not of GABA(A) receptors and gephyrin. J Neurosci 22: 4805–4813: 2002.

    PubMed  CAS  Google Scholar 

  20. Buchert M, Schneider S, Meskenaite V, Adams MT, Canaani E, Baechi T, Moelling K, and Hovens CM. The Junction-associated protein AF-6 interacts and clusters with specific Eph receptor tyrosine kinases at specialized sites of cell–cell contact in the brain. J Cell Biol 144: 361–371: 1999.

    PubMed  CAS  Google Scholar 

  21. Bukalo O, Fentrop N, Lee AY, Salmen B, Law JW, Wotjak CT, Schweizer M, Dityatev A, and Schachner M. Conditional ablation of the neural cell adhesion molecule reduces precision of spatial learning, long-term potentiation, and depression in the CA1 subfield of mouse hippocampus. J Neurosci 24: 1565–1577: 2004.

    PubMed  CAS  Google Scholar 

  22. Burette A, Khatri L, Wyszynski M, Sheng M, Ziff EB, and Weinberg RJ. Differential cellular and subcellular localization of ampa receptor-binding protein and glutamate receptor-interacting protein. J Neurosci 21: 495–503: 2001.

    PubMed  CAS  Google Scholar 

  23. Butz S, Okamoto M, and Sudhof TC. A tripartite protein complex with the potential to couple synaptic vesicle exocytosis to cell adhesion in brain. Cell 94: 773–782, 1998.

    PubMed  CAS  Google Scholar 

  24. Caillard O, Ben-Ari Y, and Gaiarsa J-L. Long-term potentiation of GABAergic synaptic transmission in neonatal rat hippocampus. J Physiol (Lond) 518: 109–119: 1999.

    CAS  Google Scholar 

  25. Caillard O, Ben-Ari Y, and Gaiarsa J-L. Mechanisms of Induction and Expression of Long-Term Depression at GABAergic Synapses in the Neonatal Rat Hippocampus. J Neurosci 19: 7568–7577: 1999.

    PubMed  CAS  Google Scholar 

  26. Cantallops I and Cline HT. Synapse formation: if it looks like a duck and quacks like a duck. Curr Biol 10: R620–R623: 2000.

    PubMed  CAS  Google Scholar 

  27. Carlisle HJ and Kennedy MB. Spine architecture and synaptic plasticity. Trends Neurosci 28: 182–187: 2005.

    PubMed  CAS  Google Scholar 

  28. Charych EI, Yu W, Li R, Serwanski DR, Miralles CP, Li X, Yang BY, Pinal N, Walikonis R, and De Blas AL. A four PDZ domain-containing splice variant form of GRIP1 is localized in GABAergic and glutamatergic synapses in the brain. J Biol Chem 279: 38978–38990: 2004.

    PubMed  CAS  Google Scholar 

  29. Chavis P and Westbrook G. Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. 411: 317–321: 2001.

    Google Scholar 

  30. Chih B, Engelman H, and Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 307: 1324–1328: 2005.

    PubMed  CAS  Google Scholar 

  31. Chih B, Engelman H, and Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 307: 1324–1328: 2005.

    PubMed  CAS  Google Scholar 

  32. Chih B, Gollan L, and Scheiffele P.Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 51: 171–178: 2006.

    PubMed  CAS  Google Scholar 

  33. Chubykin AA, Atasoy D, Etherton MR, Brose N, Kavalali ET, Gibson JR, and Sudhof TC. Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin- 1 versus neuroligin-2. Neuron 54: 919–931: 2007.

    PubMed  CAS  Google Scholar 

  34. Comoletti D, Flynn R, Jennings LL, Chubykin A, Matsumura T, Hasegawa H, Sudhof TC, and Taylor P. Characterization of the interaction of a recombinant soluble neuroligin- 1 with neurexin-1beta. J Biol Chem 278: 50497–50505: 2003.

    PubMed  CAS  Google Scholar 

  35. Comoletti D, Flynn RE, Boucard AA, Demeler B, Schirf V, Shi J, Jennings LL, Newlin HR, Sudhof TC, and Taylor P. Gene selection, alternative splicing, and post-translational processing regulate neuroligin selectivity for beta-neurexins. Biochemistry 45: 12816–12827: 2006.

    PubMed  CAS  Google Scholar 

  36. Contractor A, Rogers C, Maron C, Henkemeyer M, Swanson GT, and Heinemann SF. Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science 296: 1864–1869: 2002.

    PubMed  CAS  Google Scholar 

  37. Craig AM and Boudin H. Molecular heterogeneity of central synapses: afferent and target regulation. Nat Neurosci 4: 569–578: 2001.

    PubMed  CAS  Google Scholar 

  38. Craig AM and Kang Y. Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol 17: 43–52: 2007.

    PubMed  CAS  Google Scholar 

  39. Cremer H, Chazal G, Goridis C, and Represa A. NCAM is essential for axonal growth and fasciculation in the hippocampus. Mol Cell Neurosci 8: 323–335: 1997.

    PubMed  CAS  Google Scholar 

  40. Dalva MB, Takasu MA, Lin MZ, Shamah SM, Hu L, Gale NW, and Greenberg ME. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103: 945–956: 2000.

    PubMed  CAS  Google Scholar 

  41. Danglot L, Triller A, and Bessis A.Association of gephyrin with synaptic and extrasynaptic GABA receptors varies during development in cultured hippocampal neurons. Mol Cell Neurosci 23: 264–278: 2003.

    PubMed  CAS  Google Scholar 

  42. Davis S, Gale NW, Aldrich TH, Maisonpierre PC, Lhotak V, Pawson T, Goldfarb M, and Yancopoulos GD. Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science 266: 816–819: 1994.

    PubMed  CAS  Google Scholar 

  43. Daw MI, Chittajallu R, Bortolotto ZA, Dev KK, Duprat F, Henley JM, Collingridge GL, and Isaac JT. PDZ proteins interacting with C-terminal GluR2/3 are involved in a PKCdependent regulation of AMPA receptors at hippocampal synapses. Neuron 28: 873–886: 2000.

    PubMed  CAS  Google Scholar 

  44. Dean C and Dresbach T. Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci 29: 21-29: 2006.

    PubMed  CAS  Google Scholar 

  45. Dean C, Scholl FG, Choih J, DeMaria S, Berger J, Isacoff E, and Scheiffele P. Neurexin mediates the assembly of presynaptic terminals. Nat Neurosci 6: 708–716: 2003.

    PubMed  CAS  Google Scholar 

  46. Delling M, Wischmeyer E, Dityatev A, Sytnyk V, Veh RW, Karschin A, and Schachner M. The neural cell adhesion molecule regulates cell-surface delivery of G-proteinactivated inwardly rectifying potassium channels via lipid rafts. J Neurosci 22: 7154–7164: 2002.

    PubMed  CAS  Google Scholar 

  47. DeSouza S, Fu J, States BA, and Ziff EB. Differential palmitoylation directs the AMPA receptor-binding protein ABP to spines or to intracellular clusters. J Neurosci 22: 3493–3503: 2002.

    PubMed  CAS  Google Scholar 

  48. Conroy WG, Nai Q, Ross B, Naughton G, and Berg DK. Postsynaptic neuroligin enhances presynaptic inputs at neuronal nicotinic synapses. Dev Biol 307: 79–91: 2007.

    PubMed  CAS  Google Scholar 

  49. Dean C and Dresbach T. Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci 29: 21-29: 2006.

    PubMed  CAS  Google Scholar 

  50. Dityatev A, Dityateva G, and Schachner M. Synaptic strength as a function of postversus presynaptic expression of the neural cell adhesion molecule NCAM.Neuron 26: 207–217: 2000.

    PubMed  CAS  Google Scholar 

  51. Dityatev A, Dityateva G, Sytnyk V, Delling M, Toni N, Nikonenko I, Muller D, and Schachner M. Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses. J Neurosci 24: 9372–9382: 2004.

    PubMed  CAS  Google Scholar 

  52. Dong H, O’Brien RJ, Fung ET, Lanahan AA, Worley PF, and Huganir RL. GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature 386: 279–284: 1997.

    PubMed  CAS  Google Scholar 

  53. Dong N, Qi J, and Chen G. Molecular reconstitution of functional GABAergic synapses with expression of neuroligin-2 and GABA(A) receptors. Mol Cell Neurosci 35: 14–23, 2007.

    PubMed  CAS  Google Scholar 

  54. Dudanova I, Sedej S, Ahmad M, Masius H, Sargsyan V, Zhang W, Riedel D, Angenstein F, Schild D, Rupnik M, and Missler M. Important contribution of alpha-neurexins to Ca2+-triggered exocytosis of secretory granules. J Neurosci 26: 10599–10613: 2006.

    PubMed  CAS  Google Scholar 

  55. Dudanova I, Tabuchi K, Rohlmann A, Sudhof TC, and Missler M. Deletion of alphaneurexins does not cause a major impairment of axonal pathfinding or synapse formation. J Comp Neurol 502: 261–274: 2007.

    PubMed  CAS  Google Scholar 

  56. Durand CM, Betancur C, Boeckers TM, Bockmann J, Chaste P, Fauchereau F, Nygren G, Rastam M, Gillberg IC, Anckarsater H, Sponheim E, Goubran-Botros H, Delorme R, Chabane N, Mouren-Simeoni MC, de Mas P, Bieth E, Roge B, Heron D, Burglen L, Gillberg C, Leboyer M, and Bourgeron T. Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat Genet 39: 25–27: 2007.

    PubMed  CAS  Google Scholar 

  57. Eckhardt M, Bukalo O, Chazal G, Wang L, Goridis C, Schachner M, Gerardy-Schahn R, Cremer H, and Dityatev A. Mice deficient in thepolysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. J Neurosci 20: 5234–5244: 2000.

    PubMed  CAS  Google Scholar 

  58. Einheber S, Schnapp LM, Salzer JL, Cappiello ZB, and Milner TA. Regional and ultrastructural distribution of the alpha 8 integrin subunit in developing and adult rat brain suggests a role in synaptic function. J Comp Neurol 370: 105–134: 1996.

    PubMed  CAS  Google Scholar 

  59. El-Husseini AE, Schnell E, Chetkovich DM, Nicoll RA, and Bredt DS. PSD-95 involvement in maturation of excitatory synapses. Science 290: 1364–1368: 2000.

    PubMed  CAS  Google Scholar 

  60. Ethell IM, Irie F, Kalo MS, Couchman JR, Pasquale EB, and Yamaguchi Y. EphB/syndecan-2 signaling in dendritic spine morphogenesis. Neuron 31: 1001–1013, 2001.

    PubMed  CAS  Google Scholar 

  61. Ethell IM and Pasquale EB. Molecular mechanisms of dendritic spine development and remodeling. Prog Neurobiol 75: 161–205: 2005.

    PubMed  CAS  Google Scholar 

  62. Fazeli MS, Breen K, Errington ML, and Bliss TV. Increase in extracellular NCAM and amyloid precursor protein following induction of long-term potentiation in the dentate gyrus of anaesthetized rats. Neurosci Lett 169: 77–80: 1994.

    PubMed  CAS  Google Scholar 

  63. Feng J, Schroer R, Yan J, Song W, Yang C, Bockholt A, Cook EH, Jr., Skinner C, Schwartz CE, and Sommer SS. High frequency of neurexin 1beta signal peptide structural variants in patients with autism. Neurosci Lett 409: 10–13: 2006.

    PubMed  CAS  Google Scholar 

  64. Fiala JC, Feinberg M, Popov V, and Harris KM. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci 18: 8900–8911: 1998.

    PubMed  CAS  Google Scholar 

  65. Fischer F, Kneussel M, Tintrup H, Haverkamp S, Rauen T, Betz H, and Wassle H. Reduced synaptic clustering of GABA and glycine receptors in the retina of the gephyrin null mutant mouse. J Comp Neurol 427: 634–648: 2000.

    PubMed  CAS  Google Scholar 

  66. Flanagan JG and Vanderhaeghen P. The Ephrins and Eph Receptors in Neural Deveopment. Annu Rev Neurosci 21: 309–345: 1998.

    PubMed  CAS  Google Scholar 

  67. Frank M, Ebert M, Shan W, Phillips GR, Arndt K, Colman DR, and Kemler R. Differential expression of individual gamma-protocadherins during mouse brain development. Mol Cell Neurosci Aug; 29: 603–616: 2005.

    CAS  Google Scholar 

  68. Frank M and Kemler R. Protocadherins. Curr Opin Cell Biol 14: 557–562: 2002.

    PubMed  CAS  Google Scholar 

  69. Friedman HV, Bresler T, Garner CC, and Ziv NE. Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27: 57–69: 2000.

    PubMed  CAS  Google Scholar 

  70. Fu Z, Washbourne P, Ortinski P, and Vicini S. Functional excitatory synapses in HEK293 cells expressing neuroligin and glutamate receptors. J Neurophysiol 90: 3950–3957: 2003.

    PubMed  CAS  Google Scholar 

  71. Fujita E, Kouroku Y, Ozeki S, Tanabe Y, Toyama Y, Maekawa M, Kojima N, Senoo H, Toshimori K, and Momoi T. Oligo-astheno-teratozoospermia in mice lacking RA175/TSLC1/SynCAM/IGSF4A, a cell adhesion molecule in the immunoglobulin superfamily. Mol Cell Biol 26: 718–726: 2006.

    PubMed  CAS  Google Scholar 

  72. Futai K, Kim MJ, Hashikawa T, Scheiffele P, Sheng M, and Hayashi Y. Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin. Nat Neurosci 10: 186–195: 2007.

    PubMed  CAS  Google Scholar 

  73. Gaiarsa J-L, Caillard O, and Ben-Ari Y. Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance. Trends Neurosci 25: 564–570: 2002.

    PubMed  CAS  Google Scholar 

  74. Garner CC, Zhai RG, Gundelfinger ED, and Ziv NE. Molecular mechanisms of CNS synaptogenesis. Trends Neurosci 25: 243–251: 2002.

    PubMed  CAS  Google Scholar 

  75. Gerrow K and El-Husseini A. Cell adhesion molecules at the synapse. Front Biosci 11: 2400–2419: 2006.

    PubMed  CAS  Google Scholar 

  76. Gerrow K, Romorini S, Nabi SM, Colicos MA, Sala C, and El-Husseini A. A preformed complex of postsynaptic proteins is involved in excitatory synapse development. Neuron 49: 547–562: 2006.

    PubMed  CAS  Google Scholar 

  77. Gilbert MM and Auld VJ. Evolution of clams (cholinesterase-like adhesion molecules): structure and function during development. Front Biosci 10: 2177–2192: 2005.

    PubMed  CAS  Google Scholar 

  78. Goda Y and Davis GW. Mechanisms of synapse assembly and disassembly. Neuron 40: 243–264: 2003.

    PubMed  CAS  Google Scholar 

  79. Graf ER, Kang Y, Hauner AM, and Craig AM. Structure function and splice site analysis of the synaptogenic activity of the neurexin-1 beta LNS domain. J Neurosci 26: 4256–4265: 2006.

    PubMed  CAS  Google Scholar 

  80. Graf ER, Zhang X, Jin SX, Linhoff MW, and Craig AM. Neurexins Induce Differentiation of GABA and Glutamate Postsynaptic Specializations via Neuroligins.Cell 119: 1013–1026: 2004.

    PubMed  CAS  Google Scholar 

  81. Gubellini P, Ben-Ari Y, and Gaiarsa J-L. Activity- and age-dependent GABAergic synaptic plasticity in the developing rat hippocampus. Eur J Neurosci 14: 1937–1946, 2001.

    PubMed  CAS  Google Scholar 

  82. Harris KM, Jensen FE, and Tsao B. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci 12: 2685–2705: 1992.

    PubMed  CAS  Google Scholar 

  83. Hashimoto K and Kano M. Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron 38: 785–796: 2003.

    Google Scholar 

  84. Hayashi K, Kaufman L, Ross MD, and Klotman PE. Definition of the critical domains required for homophilic targeting of mouse sidekick molecules. FASEB J 19: 614–616, 2005.

    PubMed  CAS  Google Scholar 

  85. Hering H and Sheng M. Dendritic spines: structure, dynamics and regulation. Nat Rev Neurosci 2: 880–888: 2001.

    PubMed  CAS  Google Scholar 

  86. Holst BD, Vanderklish PW, Krushel LA, Zhou W, Langdon RB, McWhirter JR, Edelman GM, and Crossin KL. Allosteric modulation of AMPA-type glutamate receptors increases activity of the promoter for the neural cell adhesion molecule, N-CAM. Proc Natl Acad Sci U S A 95: 2597–2602: 1998.

    PubMed  CAS  Google Scholar 

  87. Howarth M.J.,- Chinnapen F, Dorrestein P.C., Gerrow K., Grandy M.R., Kelleher NL, El-Husseini A, and Ting. AY. A monovalent streptavidin with a single femtomolar biotin binding site. Nature Methods 3:267–273: 2006.

    Google Scholar 

  88. Hübschmann MV, Skladchikova G, Bock E, and Berezin V. Neural cell adhesion molecule function is regulated by metalloproteinase-mediated ectodomain release. J Neurosci Res 80: 826–837: 2005.

    PubMed  Google Scholar 

  89. Ichtchenko K, Hata Y, Nguyen T, Ullrich B, Missler M, Moomaw C, and Sudhof TC. Neuroligin 1: a splice site-specific ligand for beta-neurexins. Cell 81: 435–443: 1995.

    PubMed  CAS  Google Scholar 

  90. Ichtchenko K, Nguyen T, and Sudhof TC. Structures, alternative splicing, and neurexin binding of multiple neuroligins. J Biol Chem 271: 2676–2682: 1996.

    PubMed  CAS  Google Scholar 

  91. Inoue A and Sanes JR. Lamina-specific connectivity in the brain: regulation by Ncadherin, neurotrophins, and glycoconjugates. Science 276: 1428–1431: 1997.

    PubMed  CAS  Google Scholar 

  92. Itoh K, Ozaki M, Stevens B, and Fields RD. Activity-dependent regulation of N-cadherin in DRG neurons: differential regulation of N-cadherin, NCAM, and L1 by distinct patterns of action potentials. J Neurobiol 33: 735–748: 1997.

    PubMed  CAS  Google Scholar 

  93. Jamain S, Quach H, Betancur C, Rastam M, Colineaux C, Gillberg IC, Soderstrom H, Giros B, Leboyer M, Gillberg C, and Bourgeron T. Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat Genet 34: 27– 29: 2003.

    PubMed  CAS  Google Scholar 

  94. Jontes JD, Emond MR, and Smith SJ. In vivo trafficking and targeting of N-cadherin to nascent presynaptic terminals. J Neurosci 24: 9027–9034: 2004.

    PubMed  CAS  Google Scholar 

  95. Kamiguchi H, Hlavin ML, and Lemmon V. Role of L1 in Neural development: what the knockouts tell us. Mol Cell Neurosci 12: 48–55: 1998.

    PubMed  CAS  Google Scholar 

  96. Kayser MS, McClelland AC, Hughes EG, and Dalva MB. Intracellular and transsynaptic regulation of glutamatergic synaptogenesis by EphB receptors. J Neurosci 26: 12152–12164: 2006.

    PubMed  CAS  Google Scholar 

  97. Kennedy MB. The postsynaptic density at glutamatergic synapses. Trends Neurosci 20: 264–268: 1997.

    PubMed  CAS  Google Scholar 

  98. Kim CH, Chung HJ, Lee HK, and Huganir RL. Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression. Proc Natl Acad Sci U S A 98: 11725–11730: 2001.

    PubMed  CAS  Google Scholar 

  99. Kim E and Sheng M. PDZ domain proteins of synapses. Nat Rev Neurosci 5: 771–781, 2004.

    PubMed  CAS  Google Scholar 

  100. Kim JS, Kim HY, Kim JH, Shin HK, Lee SH, Lee YS, and Son H. Enhancement of rat hippocampal long-term potentiation by 17[beta]-estradiol involves mitogen-activated protein kinase-dependent and -independent components. Neurosci Lett 332: 65–69: 2002.

    PubMed  CAS  Google Scholar 

  101. Kim S, Burette A, Chung HS, Kwon SK, Woo J, Lee HW, Kim K, Kim H, Weinberg RJ, and Kim E. NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nat Neurosci 9: 1294–1301: 2006.

    PubMed  CAS  Google Scholar 

  102. Kirov SA, Goddard CA, and Harris KM. Age-dependence in the homeostatic upregulation of hippocampal dendritic spine number during blocked synaptic transmission. Neuropharmacology 47: 640–648: 2004.

    PubMed  CAS  Google Scholar 

  103. Kirov SA and Harris KM. Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated. Nat Neurosci 2: 878–883: 1999.

    PubMed  CAS  Google Scholar 

  104. Hoogenraad CC, Milstein AD, Ethell IM, Henkemeyer M, and Sheng M. GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking. Nat Neurosci 8: 906–915: 2005.

    PubMed  CAS  Google Scholar 

  105. Kirov SA, Petrak LJ, Fiala JC, and Harris KM. Dendritic spines disappear with chilling but proliferate excessively upon rewarming of mature hippocampus. Neuroscience 127: 69–80: 2004.

    PubMed  CAS  Google Scholar 

  106. Kneussel M and Betz H. Clustering of inhibitory neurotransmitter receptors at developing postsynaptic sites: the membrane activation model. Trends Neurosci 23: 429–435, 2000.

    PubMed  CAS  Google Scholar 

  107. Kneussel M, Brandstatter JH, Gasnier B, Feng G, Sanes JR, and Betz H. Gephyrinindependent clustering of postsynaptic GABA(A) receptor subtypes. Mol Cell Neurosci 17: 973–982: 2001.

    PubMed  CAS  Google Scholar 

  108. Kneussel M, Brandstatter JH, Laube B, Stahl S, Muller U, and Betz H. Loss of postsynaptic GABA(A) receptor clustering in gephyrin-deficient mice. J Neurosci 19: 9289–9297: 1999.

    PubMed  CAS  Google Scholar 

  109. Ko J, Kim S, Chung HS, Kim K, Han K, Kim H, Jun H, Kaang BK, and Kim E. SALM synaptic cell adhesion-like molecules regulate the differentiation of excitatory synapses. Neuron 50: 233–245: 2006.

    PubMed  CAS  Google Scholar 

  110. Konstantareas MM and Homatidis S.Chromosomal abnormalities in a series of children with autistic disorder. J Autism Dev Disord 29: 275–285: 1999.

    PubMed  CAS  Google Scholar 

  111. Kornau HC, Seeburg PH, and Kennedy MB. Interaction of ion channels and receptors with PDZ domain proteins. Curr Opin Neurobiol 7: 368–373: 1997.

    PubMed  CAS  Google Scholar 

  112. Laumonnier F, Bonnet-Brilhault F, Gomot M, Blanc R, David A, Moizard MP, Raynaud M, Ronce N, Lemonnier E, Calvas P, Laudier B, Chelly J, Fryns JP, Ropers HH, Hamel BC, Andres C, Barthelemy C, Moraine C, and Briault S. X-linked mental retardation and autism are associated with a mutation in the NLGN4 gene, a member of the neuroligin family. Am J Hum Genet 74: 552–557: 2004.

    PubMed  CAS  Google Scholar 

  113. Lee SH and Sheng M. Development of neuron-neuron synapses. Curr Opin Neurobiol 10: 125–131: 2000.

    PubMed  CAS  Google Scholar 

  114. Levi S, Grady RM, Henry MD, Campbell KP, Sanes JR, and Craig AM. Dystroglycan is selectively associated with inhibitory GABAergic synapses but is dispensable for their differentiation. J Neurosci 22: 4274–4285: 2002.

    PubMed  CAS  Google Scholar 

  115. Levi S, Logan SM, Tovar KR, and Craig AM. Gephyrin is critical for glycine receptor clustering but not for the formation of functional GABAergic synapses in hippocampal neurons. J Neurosci 24: 207–217: 2004.

    PubMed  CAS  Google Scholar 

  116. Levinson JN, Chery N, Huang K, Wong TP, Gerrow K, Kang R, Prange O, Wang YT, and El-Husseini A. Neuroligins Mediate Excitatory and Inhibitory Synapse Formation: INVOLVEMENT OF PSD-95 AND NEUREXIN-1{beta} IN NEUROLIGININDUCED SYNAPTIC SPECIFICITY. J Biol Chem 280: 17312–17319: 2005.

    PubMed  CAS  Google Scholar 

  117. Levinson JN, Chery N, Huang K, Wong TP, Gerrow K, Kang R, Prange O, Wang YT, and El-Husseini A. Neuroligins mediate excitatory and inhibitory synapse formation: involvement of PSD-95 and neurexin-1beta in neuroligin-induced synaptic specificity. J Biol Chem 280: 17312–17319: 2005.

    PubMed  CAS  Google Scholar 

  118. Li RW, Serwanski DR, Miralles CP, Li X, Charych E, Riquelme R, Huganir RL, and de Blas AL. GRIP1 in GABAergic synapses. J Comp Neurol 488: 11–27: 2005.

    PubMed  CAS  Google Scholar 

  119. Lichtman JW and Colman H. Synapse elimination and indelible memory. Neuron 25: 269–278: 2000.

    PubMed  CAS  Google Scholar 

  120. Lise MF and El-Husseini A. The neuroligin and neurexin families: from structure to function at the synapse. Cell Mol Life Sci 63: 1833–1849: 2006.

    PubMed  CAS  Google Scholar 

  121. Ko J and Kim E. Leucine-rich repeat proteins of synapses. J Neurosci Res 85: 2829–2832, 2007.

    Google Scholar 

  122. Levinson JN and El-Husseini A. Building excitatory and inhibitory synapses: balancing neuroligin partnerships. Neuron 48: 171–174: 2005.

    PubMed  CAS  Google Scholar 

  123. Luthi A, Mohajeri H, Schachner M, and Laurent JP. Reduction of hippocampal longterm potentiation in transgenic mice ectopically expressing the neural cell adhesion molecule L1 in astrocytes. J Neurosci Res 46: 1–6: 1996.

    PubMed  CAS  Google Scholar 

  124. Meyer G, Varoqueaux F, Neeb A, Oschlies M, and Brose N. The complexity of PDZ domain-mediated interactions at glutamatergic synapses: a case study on neuroligin. Neuropharmacology 47: 724–733: 2004.

    PubMed  CAS  Google Scholar 

  125. Missler M, Fernandez-Chacon R, and Sudhof TC. The making of neurexins. J Neurochem 71: 1339–1347: 1998.

    Article  PubMed  CAS  Google Scholar 

  126. Missler M, Hammer RE, and Sudhof TC.Neurexophilin binding to alpha-neurexins. A single LNS domain functions as an independently folding ligand-binding unit. J Biol Chem 273: 34716–34723: 1998.

    PubMed  CAS  Google Scholar 

  127. Missler M and Sudhof TC. Neurexins: three genes and 1001 products. Trends Genet 14: 20–26: 1998.

    PubMed  CAS  Google Scholar 

  128. Missler M, Zhang W, Rohlmann A, Kattenstroth G, Hammer RE, Gottmann K, and Sudhof TC. Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 423: 939–948: 2003.

    PubMed  CAS  Google Scholar 

  129. Muller D, Wang C, Skibo G, Toni N, Cremer H, Calaora V, Rougon G, and Kiss JZ. PSA-NCAM is required for activity-induced synaptic plasticity. Neuron 17: 413–422, 1996.

    PubMed  CAS  Google Scholar 

  130. Murase S, Mosser E, and Schuman EM. Depolarization drives beta-Catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 35: 91–105, 2002.

    PubMed  CAS  Google Scholar 

  131. Nam CI and Chen L. Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proc Natl Acad Sci U S A 102: 6137–6142: 2005.

    PubMed  CAS  Google Scholar 

  132. Nguyen DN, Liu Y, Litsky ML, and Reinke R. The sidekick gene, a member of the immunoglobulin superfamily, is required for pattern formation in the Drosophila eye. Development 124: 3303–3312: 1997.

    PubMed  CAS  Google Scholar 

  133. Niethammer P, Delling M, Sytnyk V, Dityatev A, Fukami K, and Schachner M. Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J Cell Biol 157: 521–532: 2002.

    PubMed  CAS  Google Scholar 

  134. Nishimura SL, Boylen KP, Einheber S, Milner TA, Ramos DM, and Pytela R. Synaptic and glial localization of the integrin alphavbeta8 in mouse and rat brain. Brain Res 791: 271–282: 1998.

    PubMed  CAS  Google Scholar 

  135. O’Brien RJ, Lau LF, and Huganir RL. Molecular mechanisms of glutamate receptor clustering at excitatory synapses. Curr Opin Neurobiol 8: 364–369: 1998.

    PubMed  CAS  Google Scholar 

  136. Osten P, Khatri L, Perez JL, Kohr G, Giese G, Daly C, Schulz TW, Wensky A, Lee LM, and Ziff EB. Mutagenesis reveals a role for ABP/GRIP binding to GluR2 in synaptic surface accumulation of the AMPA receptor. Neuron 27: 313–325: 2000.

    PubMed  CAS  Google Scholar 

  137. Park M, Salgado JM, Ostroff L, Helton TD, Robinson CG, Harris KM, and Ehlers MD. Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52: 817–830: 2006.

    PubMed  CAS  Google Scholar 

  138. Peng J, Kim MJ, Cheng D, Duong DM, Gygi SP, and Sheng M. Semiquantitative proteomic analysis of rat forebrain postsynaptic density fractions by mass spectrometry. J Biol Chem 279: 21003–21011: 2004.

    PubMed  CAS  Google Scholar 

  139. Petrak LJ, Harris KM, and Kirov SA. Synaptogenesis on mature hippocampal dendrites occurs via filopodia and immature spines during blocked synaptic transmission. J Comp Neurol 484: 183–190: 2005.

    PubMed  Google Scholar 

  140. Petrenko AG, Ullrich B, Missler M, Krasnoperov V, Rosahl TW, and Sudhof TC. Structure and evolution of neurexophilin. J Neurosci 16: 4360–4369: 1996.

    PubMed  CAS  Google Scholar 

  141. Pierce JP and Mendell LM. Quantitative ultrastructure of Ia boutons in the ventral horn: scaling and positional relationships. J Neurosci 13: 4748–4763: 1993

    PubMed  CAS  Google Scholar 

  142. Pinkstaff JK, Detterich J, Lynch G, and Gall C. Integrin subunit gene expression is regionally differentiated in adult brain. J Neurosci 19: 1541–1556: 1999.

    PubMed  CAS  Google Scholar 

  143. Prange O, Wong TP, Gerrow K, Wang YT, and El-Husseini A. A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin. Proc Natl Acad Sci U S A 101: 13915–13920: 2004.

    PubMed  CAS  Google Scholar 

  144. Rao A, Kim E, Sheng M, and Craig AM. Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture. J Neurosci 18: 1217–1229: 1998.

    PubMed  CAS  Google Scholar 

  145. Romorini S, Piccoli G, Jiang M, Grossano P, Tonna N, Passafaro M, Zhang M, and Sala C. A functional role of postsynaptic density-95-guanylate kinase-associated protein complex in regulating Shank assembly and stability to synapses. J Neurosci 24: 9391–9404: 2004.

    PubMed  CAS  Google Scholar 

  146. Rozic-Kotliroff G and Zisapel N. Ca2+ -dependent splicing of neurexin IIalpha. Biochem Biophys Res Commun 352: 226–230: 2007.

    PubMed  CAS  Google Scholar 

  147. Rubenstein JL and Merzenich MM. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2: 255–267: 2003.

    PubMed  CAS  Google Scholar 

  148. udenko G, Nguyen T, Chelliah Y, Sudhof TC, and Deisenhofer J. The structure of the ligand-binding domain of neurexin Ibeta: regulation of LNS domain function by alternative splicing. Cell 99: 93–101: 1999.

    Google Scholar 

  149. Rutishauser U. Influences of the neural cell adhesion molecule on axon growth and guidance. J Neurosci Res 13: 123–131: 1985.

    PubMed  CAS  Google Scholar 

  150. Saghatelyan AK, Nikonenko AG, Sun M, Rolf B, Putthoff P, Kutsche M, Bartsch U, Dityatev A, and Schachner M. Reduced GABAergic transmission and number of hippocampal perisomatic inhibitory synapses in juvenile mice deficient in the neural cell adhesion molecule L1. Mol Cell Neurosci 26: 191–203: 2004.

    PubMed  CAS  Google Scholar 

  151. Sakurai T, Ramoz N, Reichert JG, Corwin TE, Kryzak L, Smith CJ, Silverman JM, Hollander E, and Buxbaum JD. Association analysis of the NrCAM gene in autism and in subsets of families with severe obsessive-compulsive or self-stimulatory behaviors. Psychiatr Genet 16: 251–257: 2006.

    PubMed  Google Scholar 

  152. Sala C, Piech V, Wilson NR, Passafaro M, Liu G, and Sheng M. Regulation of dendritic spine morphology and synaptic function by Shank and Homer.Neuron 31: 115–130, 2001.

    PubMed  CAS  Google Scholar 

  153. Sala C, Roussignol G, Meldolesi J, and Fagni L. Key role of the postsynaptic density scaffold proteins Shank and Homer in the functional architecture of Ca2+ homeostasis at dendritic spines in hippocampal neurons. J Neurosci 25: 4587–4592: 2005.

    PubMed  CAS  Google Scholar 

  154. Sanes JR and Lichtman JW. Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22: 389–442: 1999.

    PubMed  CAS  Google Scholar 

  155. Sara Y, Biederer T, Atasoy D, Chubykin A, Mozhayeva MG, Sudhof TC, and Kavalali ET. Selective capability of SynCAM and neuroligin for functional synapse assembly. J Neurosci 25: 260–270: 2005.

    PubMed  CAS  Google Scholar 

  156. Sara Y, Biederer T, Atasoy D, Chubykin A, Mozhayeva MG, Sudhof TC, and Kavalali ET. Selective capability of SynCAM and neuroligin for functional synapse assembly. J Neurosci 25: 260–270: 2005.

    PubMed  CAS  Google Scholar 

  157. Scheiffele P, Fan J, Choih J, Fetter R, and Serafini T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101: 657–669, 2000.

    PubMed  CAS  Google Scholar 

  158. Scholl FG and Scheiffele P. Making connections: cholinesterase-domain proteins in the CNS. Trends Neurosci 26: 618–624: 2003.

    PubMed  CAS  Google Scholar 

  159. Schuster T, Krug M, Hassan H, and Schachner M. Increase in proportion of hippocampalspine synapses expressing neural cell adhesion molecule NCAM180 following long-term potentiation. J Neurobiol 37: 359–372: 1998.

    PubMed  CAS  Google Scholar 

  160. Senkov O, Sun M, Weinhold B, Gerardy-Schahn R, Schachner M, and Dityatev A. Polysialylated neural cell adhesion molecule is involved in induction of long-term potentiation and memory acquisition and consolidation in a fear-conditioning paradigm. 26: 10888–109898: 2006.

    PubMed  CAS  Google Scholar 

  161. Serafini T. An old friend in a new home: cadherins at the synapse. Trends Neurosci 20: 322–323: 1997.

    PubMed  CAS  Google Scholar 

  162. Sheng M and Kim MJ. Postsynaptic signaling and plasticity mechanisms. Science 298: 776–780: 2002.

    PubMed  CAS  Google Scholar 

  163. Sheng M and Sala C. PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci 24: 1–29: 2001.

    PubMed  CAS  Google Scholar 

  164. Shingai T, Ikeda W, Kakunaga S, Morimoto K, Takekuni K, Itoh S, Satoh K, Takeuchi M, Imai T, Monden M, and Takai Y. Implications of nectin-like molecule-2/IGSF4/RA175/SgIGSF/TSLC1/SynCAM1 in cell–cell adhesion and transmembrane protein localization in epithelial cells. J Biol Chem 278: 35421–35427: 2003.

    PubMed  CAS  Google Scholar 

  165. Sia GM, Beique JC, Rumbaugh G, Cho R, Worley PF, and Huganir RL. Interaction of the N-Terminal domain of the AMPA receptor GluR4 subunit with the neuronal pentraxin NP1 mediates GluR4 synaptic recruitment. Neuron 55: 87–102: 2007.

    PubMed  CAS  Google Scholar 

  166. Song JY, Ichtchenko K, Sudhof TC, and Brose N. Neuroligin 1 is a postsynaptic celladhesion molecule of excitatory synapses. Proc Natl Acad Sci U S A 96: 1100–1105, 1999.

    PubMed  CAS  Google Scholar 

  167. Sons MS, Busche N, Strenzke N, Moser T, Ernsberger U, Mooren FC, Zhang W, Ahmad M, Steffens H, Schomburg ED, Plomp JJ, and Missler M. alpha-Neurexins are required for efficient transmitter release and synaptic homeostasis at the mouse neuromuscular junction. Neuroscience 138: 433–446: 2006.

    PubMed  CAS  Google Scholar 

  168. Spacek J and Harris KM. Trans-endocytosis via spinules in adult rat hippocampus. J Neurosci 24: 4233–4241: 2004.

    PubMed  CAS  Google Scholar 

  169. Sperry RW. Chemoaffinity in the orderly growth of nerve fibre patterns and connections. Proc Natl Acad Sci U S A 50: 703–710: 1963.

    PubMed  CAS  Google Scholar 

  170. Staubli U, Chun D, and Lynch G. Time-dependent reversal of long-term potentiation by an integrin antagonist. J Neurosci 18: 3460–3469: 1998.

    PubMed  CAS  Google Scholar 

  171. Stoenica L, Senkov O, Gerardy-Schahn R, Weinhold B, Schachner M, and Dityatev A. In vivo synaptic plasticity in the dentate gyrus of mice deficient in the neural cell adhesion molecule NCAM or its polysialic acid. Eur J Neurosci 23: 2255–2264: 2006.

    PubMed  Google Scholar 

  172. Sugita S, Saito F, Tang J, Satz J, Campbell K, and Sudhof TC. A stoichiometric complex of neurexins and dystroglycan in brain. J Cell Biol 154: 435–445: 2001.

    PubMed  CAS  Google Scholar 

  173. Sugiyama J, Bowen DC, and Hall ZW. Dystroglycan binds nerve and muscle agrin. Neuron 13: 103–115: 1994.

    PubMed  CAS  Google Scholar 

  174. Sytnyk V, Leshchyns’ka I, Dityatev A, and Schachner M. Trans-Golgi network delivery of synaptic proteins in synaptogenesis. J Cell Sci 117: 381–388: 2004.

    PubMed  CAS  Google Scholar 

  175. Szatmari P, Paterson AD, Zwaigenbaum L, Roberts W, Brian J, Liu XQ, Vincent JB, Skaug JL, Thompson AP, Senman L, Feuk L, Qian C, Bryson SE, Jones MB, Marshall CR, Scherer SW, Vieland VJ, Bartlett C, Mangin LV, Goedken R, Segre A, Pericak-Vance MA, Cuccaro ML, Gilbert JR, Wright HH, Abramson RK, Betancur C, Bourgeron T, Gillberg C, Leboyer M, Buxbaum JD, Davis KL, Hollander E, Silverman JM, Hallmayer J, Lotspeich L, Sutcliffe JS, Haines JL, Folstein SE, Piven J, Wassink TH, Sheffield V, Geschwind DH, Bucan M, Brown WT, Cantor RM, Constantino JN, Gilliam TC, Herbert M, Lajonchere C, Ledbetter DH, Lese-Martin C, Miller J, Nelson S, Samango-Sprouse CA, Spence S, State M, Tanzi RE, Coon H, Dawson G, Devlin B, Estes A, Flodman P, Klei L, McMahon WM, Minshew N, Munson J, Korvatska E, Rodier PM, Schellenberg GD, Smith M, Spence MA, Stodgell C, Tepper PG, Wijsman EM, Yu CE, Roge B, Mantoulan C, Wittemeyer K, Poustka A, Felder B, Klauck SM, Schuster C, Poustka F, Bolte S, Feineis-Matthews S, Herbrecht E, Schmotzer G, Tsiantis J, Papanikolaou K, Maestrini E, Bacchelli E, Blasi F, Carone S, Toma C, Van Engeland H, de Jonge M, Kemner C, Koop F, Langemeijer M, et al. Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nat Genet 39: 319–328: 2007.

    PubMed  CAS  Google Scholar 

  176. Takasu MA, Dalva MB, Zigmond RE, and Greenberg ME. Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 295: 491–495: 2002.

    PubMed  CAS  Google Scholar 

  177. Taniguchi H, Gollan L, Scholl FG, Mahadomrongkul V, Dobler E, Limthong N, Peck M, Aoki C, and Scheiffele P. Silencing of neuroligin function by postsynaptic neurexins. J Neurosci 27: 2815–2824: 2007.

    PubMed  CAS  Google Scholar 

  178. Togashi H, Abe K, Mizoguchi A, Takaoka K, Chisaka O, and Takeichi M. Cadherin regulates dendritic spine morphogenesis. Neuron 35: 77–89: 2002.

    PubMed  CAS  Google Scholar 

  179. Torres R, Firestein BL, Dong H, Staudinger J, Olson EN, Huganir RL, Bredt DS, Gale NW, and Yancopoulos GD. PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron 21: 1453–1463: 1998.

    PubMed  CAS  Google Scholar 

  180. Ullrich B, Ushkaryov YA, and Sudhof TC. Cartography of neurexins: more than 1000 isoforms generated by alternative splicing and expressed in distinct subsets of neurons. Neuron 14: 497–507: 1995.

    PubMed  CAS  Google Scholar 

  181. Ushkaryov YA, Hata Y, Ichtchenko K, Moomaw C, Afendis S, Slaughter CA, and Sudhof TC. Conserved domain structure of beta-neurexins. Unusual cleaved signal sequences in receptor-like neuronal cell-surface proteins. J Biol Chem 269: 11987–11992, 1994.

    PubMed  CAS  Google Scholar 

  182. Ushkaryov YA, Petrenko AG, Geppert M, and Sudhof TC. Neurexins: synaptic cell surface proteins related to the alpha-latrotoxin receptor and laminin. Science 257: 50–56, 1992.

    PubMed  CAS  Google Scholar 

  183. Vaithianathan T, Matthias K, Bahr B, Schachner M, Suppiramaniam V, Dityatev A, and Steinhauser C. Neural cell adhesion molecule-associated polysialic acid potentiates alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor currents. J Biol Chem 279: 47975–47984: 2004.

    PubMed  CAS  Google Scholar 

  184. Varoqueaux F, Aramuni G, Rawson RL, Mohrmann R, Missler M, Gottmann K, Zhang W, Sudhof TC, and Brose N. Neuroligins determine synapse maturation and function. Neuron 51: 741–754: 2006.

    PubMed  CAS  Google Scholar 

  185. Varoqueaux F, Jamain S, and Brose N. Neuroligin 2 is exclusively localized to inhibitorysynapses. Eur J Cell Biol 83: 449–456: 2004.

    PubMed  CAS  Google Scholar 

  186. Vaughn JE. Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 3: 255–285: 1989.

    PubMed  CAS  Google Scholar 

  187. Vogt AK, Brewer GJ, Decker T, Bocker-Meffert S, Jacobsen V, Kreiter M, Knoll W, and Offenhausser A. Independence of synaptic specificity from neuritic guidance. Neuroscience 134: 783–790: 2005.

    PubMed  CAS  Google Scholar 

  188. Walikonis RS, Jensen ON, Mann M, Provance DW, Jr., Mercer JA, and Kennedy MB. Identification of proteins in the postsynaptic density fraction by mass spectrometry. J Neurosci 20: 4069–4080: 2000.

    PubMed  CAS  Google Scholar 

  189. Wang CY, Chang K, Petralia RS, Wang YX, Seabold GK, and Wenthold RJ. A novel family of adhesion-like molecules that interacts with the NMDA receptor. J Neurosci 26: 2174–2183: 2006.

    PubMed  CAS  Google Scholar 

  190. Washbourne P, Bennett JE, and McAllister AK. Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nat Neurosci 5: 751–759: 2002.

    PubMed  CAS  Google Scholar 

  191. Washbourne P, Dityatev A, Scheiffele P, Biederer T, Weiner JA, Christopherson KS, and El-Husseini A. Cell Adhesion Molecules in Synapse Formation. J Neurosci 24: 9244–9249: 2004.

    PubMed  CAS  Google Scholar 

  192. Weiner JA, Wang X, Tapia JC, and Sanes JR. Gamma protocadherins are required for synaptic development in the spinal cord. Proc Natl Acad Sci U S A 102: 8–14: 2005.

    PubMed  CAS  Google Scholar 

  193. Williamson RA, Henry MD, Daniels KJ, Hrstka RF, Lee JC, Sunada Y, Ibraghimov-Beskrovnaya O, and Campbell KP. Dystroglycan is essential for early embryonic development:disruption of Reichert’s membrane in Dag1-null mice. Hum Mol Genet 6: 831–841: 1997.

    PubMed  CAS  Google Scholar 

  194. Wilson DA, Best AR, and Sullivan RM. Plasticity in the olfactory system: lessons for the neurobiology of memory. Neuroscientist 10: 513–524: 2004.

    PubMed  CAS  Google Scholar 

  195. Xiao P, Bahr BA, Staubli U, Vanderklish PW, and Lynch G. Evidence that matrix recognition contributes to stabilization but not induction of LTP. Neuroreport 2: 461–464, 1991.

    PubMed  CAS  Google Scholar 

  196. Yamagata M and Sanes JR. Target-independent diversification and target-specific projection of chemically defined retinal ganglion cell subsets. Development 121: 3763–3776: 1995.

    PubMed  CAS  Google Scholar 

  197. Yamagata M, Sanes JR, and Weiner JA. Synaptic adhesion molecules. Curr Opin Cell Biol 15: 621–632: 2003.

    PubMed  CAS  Google Scholar 

  198. Yamagata M, Weiner JA, and Sanes JR. Sidekicks: synaptic adhesion molecules that promote lamina-specific connectivity in the retina. Cell 110: 649–660: 2002.

    PubMed  CAS  Google Scholar 

  199. Zeng X, Sun M, Liu L, Chen F, Wei L, and Xie W. Neurexin-1 is required for synapse formation and larvae associative learning in Drosophila. FEBS Lett 581: 2509–2516, 2007.

    PubMed  CAS  Google Scholar 

  200. Zhang W, Rohlmann A, Sargsyan V, Aramuni G, Hammer RE, Sudhof TC, and Missler M. Extracellular domains of alpha-neurexins participate in regulating synaptic transmission by selectively affecting N- and P/Q-type Ca2+ channels. J Neurosci 25: 4330–4342, 2005.

    PubMed  CAS  Google Scholar 

  201. Ziv NE and Smith SJ. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17: 91–102: 1996.

    PubMed  CAS  Google Scholar 

  202. Zoghbi HY. Postnatal neurodevelopmental disorders: meeting at the synapse? Science 302: 826–830: 2003.

    PubMed  CAS  Google Scholar 

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  1. Department of Psychiatry, University of British Columbia, Vancouver, British Columbia

    Alaa El-Husseini

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    Johannes W. Hell

  2. Department of Neurobiology, Duke University Medical Center, Box 3209, Durham, NC 27710

    Michael D. Ehlers

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El-Husseini, A. (2008). Adhesion Molecules at the Synapse. In: Hell, J.W., Ehlers, M.D. (eds) Structural And Functional Organization Of The Synapse. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-77232-5_7

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